High sugar intake from sugar‐sweetened beverages is associated with prevalence of untreated decay in US adults: NHANES 2013–2016

Abstract Objectives To assess the association between sugar from sugar‐sweetened beverages (SSBs) and untreated decay in permanent teeth and calculate the cost burden of sugar from SSBs on untreated decay in US adults. Methods Cross‐sectional data from the 2013–2014 and 2015–2016 cycles of the National Health and Nutrition Examination Survey (NHANES) were analysed in 2020 (n = 9001 adults aged ≥20). Multivariable analyses assessed sugar intake from SSB consumption with the presence of untreated decay in permanent teeth and number of untreated decayed teeth. Population attributable risk was used to estimate the cost burden arising from SSBs on untreated decay in US adults. Results One fourth (25.1%) of US adults had untreated dental decay, and higher prevalence was observed among those with low income, low education and race/ethnicity of non‐Hispanic Black. Overall, 53% of adults reported no intake of SSBs. For the remaining 47%, the median 24‐h intake was 46.8 g of sugar from SSBs. The adjusted prevalence ratio (PR) for untreated decay was 1.3 (95% confidence interval [CI] 1.1–1.5) for consumption of 46.8 g or more of sugar from SSBs compared to those reporting no sugar from SSBs. Number of untreated decayed teeth increased with sugar intake from SSBs from lowest to highest tertile: 0.1, (p = .35); 0.4, (p = .006); and 0.6, (p < .001). The cost burden of untreated decay attributable to SSBs in US adults is estimated conservatively at $1.6 billion USD. Conclusions Community level interventions directed at sugar from SSBs are justified to address disparities in the burden of untreated dental decay.


| INTRODUC TI ON
Untreated dental decay is recognized as a global problem affecting all age groups. 1,2 This condition represents not only the outcome of a multifactorial disease process (dental caries), the lack of treatment can also indicate a failure to meet the need for dental care. In many respects, the burden of untreated dental decay in a population can frame a call to action for all stakeholders in the dental service delivery system. 3 In order to make appropriate policy changes, population-level assessments that account for social and demographic factors must be examined with respect to untreated dental decay. [4][5][6][7] This paper provides actionable data to drive policy development around the role of grams of sugar from sugar-sweetened beverages (SSBs) and untreated dental decay using population-level data for adults in the United States.
Published research has made a strong case for a causal association between sugar from SSBs and dental caries. 8 As a disease process, dental caries is the interplay of diet and bacterial factors to create a low pH microenvironment where demineralization of tooth structure outpaces remineralization over time. 9 Undoubtedly, fermentable carbohydrates provide a causal pathway for dental caries. [10][11][12] Studies have established the importance of sugar intake from beverages. 8,13 While sugar from other sources (i.e., candy, bakery items and chewing gum) and other fermentable carbohydrates contribute to dental decay, sugar-sweetened beverages (SSBs) have been identified by policy makers as a focus for action. [14][15][16][17][18][19][20] It should be noted that in addition to the role sugar plays in dental disease, the World Health Organization has recommended reductions in sugar intake for adults and children to address a broad range of health issues arising from a role for sugar in poor dietary quality and obesity. 21 In 2019, expenditures for dental care in the United States were estimated at $143 billion (US dollars). 22 Unmet need for treatment represents an additional burden that is not captured in expenditure data. Therefore, this study investigated the association between sugar from SSBs and untreated dental decay using data from the 2013-2016 National Health and Nutrition Examination Survey (NHANES). The aim of this study was twofold. First, to test the association between grams of sugar consumed from SSBs and (a) the presence or absence of untreated decay; and (b) the number of untreated decayed teeth. Second, in order to frame the policy implications, population attributable risk (PAR) per cent was used to estimate treatment costs. As a policy tool, 23 PAR provides a simple estimation of the burden of untreated dental decay attributable to sugar from SSB consumption among US adults. Figure 1 shows how the study sample was derived in 2019 from the public-use data files for two cycles of NHANES: 2013-2016. NHANES is a public-use de-identified data set containing information on behavioural, demographic and environmental characteristics. In additional to these characteristics, the cross-sectional NHANES survey conducted household interviews and standard oral health examinations. All observations were weighted to a representative sample of the noninstitutionalized, civilian, household population of the United States.

| Outcomes
Analysis was limited to persons 20 years and older with at least 1 permanent tooth. For these individuals, each tooth surface was examined and scored in NHANES by calibrated, licensed dentists. 24 Tooth level scores were summed to provide an individual score representing the number of permanent decayed, missing and filled teeth (DMFT). In the dental protocol, untreated decay was assigned when cavitation at the dentine level was present at the exam- Grams (g) of sugar from SSBs was assessed as a categorical variable in two ways, using four levels to examine the presence of a dose-response pattern and using three levels to simplify the findings for policy development. In both approaches, intake of 0 g of sugar from SSBs was used as the reference group and values were rounded to one decimal place for simplicity of presentation. At four levels, the study sample with >0 intake of sugar from SSBs was defined by using tertiles. The four levels were zero, >0 but <34.8 g, 34.8 g to 73.9 g, and 74.0 g or greater. The data pattern was simplified to three levels for the calculation of population attributable risk, by splitting the group with non-zero intake of sugar from SSBs at the median.
The three levels for this were as follows: 0 g of sugar from SSBs; more than 0 but <46.8 g; and 46.8 g or more of sugar from SSBs.
As a frame of reference, a typical 12 oz sugar-sweetened soft drink contains 39 g of sugar and a 20 oz soft drink contains 65 g of sugar.
Covariates of interest available in NHANES were smoking status, age, self-reported race/ethnicity, gender, household income level as measured through the federal poverty income ratio-a ratio of family income to poverty guidelines-as ≤130%, 131%-350% and >350%, education level (identified by highest level attained: less than high school, high school graduation, some college, college and above), and dental visit behaviour (as whether or not there was a dental office visit in the past 12 months). Smoking status was self-reported as current, former or never.

| Statistical analysis
Methods to account for the sampling weights were incorporated into data analysis by using STATA version 13.1. Untreated decay was The PAR per cent serves as a policy tool that provides an estimate of the amount of untreated decay that could be averted if sugar intake from SSBs was reduced. 23 To be meaningful the PAR The relative increment in number of untreated decayed teeth was derived from the negative binomial model. 29 In this manner, a conservative estimate of treatment costs to address a single surface lesion attributable to sugar from SSBs was derived for US adults where the base cost would be $322 to restore one tooth and an additional $125 to restore a second tooth at the same visit. These estimates include the fee for a comprehensive examination and fullmouth series of radiographs.

| RE SULTS
The sample consisted of 9001 adults with complete data for the variables of interest (Figure 1). Table 1  Regression results are displayed in Table 2. The first set of columns present prevalence ratios (PRs) and 95 per cent CIs for the Poisson likelihood of having at least one tooth with untreated decay.
The last set of columns present the regression results for a negative binomial model estimating the association with mean number of untreated decayed teeth. Both models show consistent results.  The models ( PAR results shown in Table 3 were estimated by using the prevalence ratio from a multivariable model with non-zero sugar intake divided at the median. In this model, the adjusted prevalence was 30 per cent greater for untreated decay for those consuming more than the median amount of sugar from SSBs compared to those consuming no sugar from beverages (PR 1.3, 95% CI: 1.1, 1.5). PAR results suggest that 6.8 per cent of US adults had untreated decay attributable to sugar intake from SSBs (Table 3). This translates to 3.6 million people who had untreated decay because of high SSB consumption. Estimates from the negative binomial model show that high SSB consumption contributed to an average of two additional decayed teeth among those with untreated decay. Table 3 shows that the cost of treatment can be estimated from these data. The economic impact is conservatively estimated at $1.6 billion (USD).

| DISCUSS ION
These analyses support the hypotheses that grams of sugar from These cross-sectional findings are consistent with prospective findings for sugar from SSBs 13 as well as social determinants 31-33 and smoking. 34,35 Our results show that untreated decay follows strong socioeconomic indicators-those with low income, and low education have higher burdens. Also, those who are non-Hispanic Black have burdens that are significantly greater than those who are non-Hispanic White. These results are consistent with prior work that shows that tap water avoidance, which leads to SSB consumption is highest in these groups due to marginalization and histories of inequitable access to clean water. 36

TA B L E 1 (Continued)
Dental caries is a multifactorial disease process and while the literature clearly links sugar exposure to dental caries, only a few observational studies provide evidence among adults. 8

Work in
Finland has established that sugar intake is linked to adult caries increment in a linear dose-response manner. 39 Two recent studies used data from NHANES. One focused on US adults in the 2013-2014 cycle of NHANES and showed an association in those older than age 30 between dental caries experience measured as DMFT and dietary patterns that favoured SSBs and sandwiches. 40 The second study 41  SSBs. 16 The concept of a tax on sugar from SSBs, based largely on beneficial effects arising from reduced intake of sugar on the population, has been widely promoted in public health policy circles. [14][15][16]20 However, critics argue that such a tax has the potential to be 'regressive' by adversely impacting the segment of the population that is least able to bear the additional cost. Allcott et al. 14 point out that policy can be tailored so that revenues from the tax are ear-marked for programmes that can benefit low-income populations, as was done in Philadelphia. 17 This study used data from a large, nationally representative sample of the US adult population with standardized measures for dental caries and grams of sugar from SSBs. This provides an opportunity for estimating population-level burden using accurate estimates of prevalence and exposure. Our findings for untreated dental decay support the recommendations from both the AHA and USDA to limit sugar consumption to below 35 g of sugar. Furthermore, we found a TA B L E 2 Multivariable models for association between sugar intake from sugar-sweetened beverages and selected confounders with untreated decay among US Adults, NHANES 2013-2016 dose-response association for a higher prevalence of untreated decay in US adults and a higher predicted number of untreated decayed teeth for those with more than 35 g of sugar from SSBs. Limitations in this study include use of cross-sectional data and self-reported 24-h dietary recall. Total sugar and frequency of consumption are highly correlated, and this study cannot disaggregate these factors.
We cannot rule out that frequency of consumption is more important than total amount of sugar consumed. 12  However, presence of untreated decayed teeth represents a constellation of at least three components-a disease process; a behavioural component; and the ability to obtain dental care when sought. Dental care seeking was measured by dental visits in the past year. While significant, we are only able to speculate on the intersectionality of socioeconomic status, care-seeking behaviour, and access to care. 46 This study is unable to completely untangle these components.

| CON CLUS ION
The burden of untreated decay attributable to intake of sugar from SSBs is clearly present in the US adult population identified as having a low income, low education attainment and/or who identified as non-Hispanic Black. Treatment costs attributable to SSB consumption exceed $1.6 billion in US adults. As a policy lever, revenue  Adjusted for same variables as listed in Table 2 (smoking, age, sex, race/ethnicity, poverty income ratio, education and dental visit in past year). generated by a tax on SSBs can be justified to support local communities in addressing the social inequities that contribute to untreated dental decay in underserved population groups.

ACK N OWLED G EM ENT
The authors acknowledge Dr. Qiang Wu for his help in coding of NHANES variables for clinical caries status.

CO N FLI C T O F I NTE R E S T
None to declare.

AUTH O R CO NTR I B UTI O N S
MEM, HL and AYR contributed to the conception, design, data acquisition and initially drafted the approach for this paper. HL conducted the data analysis and provided interpretation of the findings.

DATA AVA I L A B I L I T Y S TAT E M E N T
NHANES is publicly available. Requests for access to the methods for computing grams of sugar from SSB intake can be directed to AYR.